Rethinking the fear circuit: The central nucleus of the amygdala is required for the acquisition, consolidation, and expression of pavlovian fear conditioning

Journal of Neuroscience

Volumn 26, Issue 48, 2006, Pages 12387-12396

  Wilensky, Ann E ^a   Schafe, Glenn E ^b   Kristensen, Morten P ^a   LeDoux, Joseph E ^a  

^a NEW YORK UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; Anisomycin; Central nucleus; Consolidation; Fear conditioning; Muscimol

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; ANISOMYCIN; MUSCIMOL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; FEAR; LEARNING; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT; SENSORY STIMULATION; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; FEAR; MALE; NERVE NET; RATS; RATS, SPRAGUE-DAWLEY; THINKING;

EID: 33845243380     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4316-06.2006     Document Type: Article

References (66)

1. Alberini CM, Ghirardi M, Huang YY, Nguyen PV, Kandel ER (1995) A molecular switch for the consolidation of long-term memory: cAMP-inducible gene expression. Ann NY Acad Sci 758:261-286.
2. Amorapanth P, LeDoux JE, Nader K (2000) Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 3:74-79.
3. Anglada-Figueroa D, Quirk GJ (2005) Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25:9680-9685.
4. Applegate CD, Frysinger RC, Kapp BS, Gallagher M (1982) Multiple unit activity recorded from amygdala central nucleus during Pavlovian heart rate conditioning in rabbit. Brain Res 238:457-462.
5. Applegate CD, Kapp BS, Underwood MD, McNall CL (1983) Autonomic and somatomotor effects of amygdala central N. stimulation in awake rabbits. Physiol Behav 31:353-360.
6. Arikan R, Blake NM, Erinjeri JP, Woolsey TA, Giraud L, Highstein SM (2002) A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy. J Neurosci Methods 118:51-57.
7. Bahar A, Samuel A, Hazvi S, Dudai Y (2003) The amygdalar circuit that acquires taste aversion memory differs from the circuit that extinguishes it. Eur J Neurosci 17:1527-1530.
8. Bailey DJ, Kim JJ, Sun W, Thompson RF, Helmstetter FJ (1999) Acquisition of fear conditioning in rats requires the synthesis of mRNA in the amygdala. Behav Neurosci 113:276-282.
9. Bernard JF, Besson JM (1990) The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 63:473-490.
10. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8:229-242.
11. Cahill L, Weinberger NM, Roozendaal B, McGaugh JL (1999) Is the amygdala a locus of "conditioned fear"? Some questions and caveats. Neuron 23:227-228.
12. Campeau S, Davis M (1995) Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15:2301-2311.
13. Doron NN, LeDoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412:383-409.
14. Doyère V, Schafe GE, Sigurdsson T, LeDoux JE (2003) Long-term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala. Eur J Neurosci 17:2703-2715.
15. Edeline JM, Hars B, Hennevin E, Cotillon N (2002) Muscimol diffusion after intracerebral microinjections: a reevaluation based on electrophysiological and autoradiographic quantifications. Neurobiol Learn Mem 78:100-124.
16. Fanselow MS, Kim JJ (1994) Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphonovaleric acid to the basolateral amygdala. Behav Neurosci 108:210-212.
17. Goosens KA, Maren S (2001) Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem 8:148-155.
18. Helmstetter FJ (1992) Contribution of the amygdala to learning and performance of conditional fear. Physiol Behav 51:1271-1276.
19. Helmstetter FJ, Bellgowan PS (1994) Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats. Behav Neurosci 108:1005-1009.
20. Hitchcock JM, Davis M (1991) Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm. Behav Neurosci 105:826-842.
21. Hopkins DA, Holstege G (1978) Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp Brain Res 32:529-547.
22. Jasmin L, Burkey AR, Card JP, Basbaum AI (1997) Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-)parabrachio-amygdaloid, in the rat. J Neurosci 17:3751-3765.
23. Kapp BS, Frysinger RC, Gallagher M, Haselton JR (1979) Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 23:1109-1117.
24. Kapp BS, Wilson A, Pascoe J, Supple W, Whalen PJ (1990) Aneuroanatomical systems analysis of conditioned bradycardia in the rabbit. In: Learning and computational neuroscience: foundations of adaptive networks (Gabriel M, Moore J, eds), pp 53-90. Cambridge, MA: MIT.
25. Kim M, Davis M (1993) Electrolytic lesions of the amygdala block acquisition and expression of fear-potentiated startle even with extensive training but do not prevent reacquisition. Behav Neurosci 107:580-595.
26. Koo JW, Han JS, Kim JJ (2004) Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci 24:7654-7662.
27. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
28. LeDoux JE, Ruggiero DA, Reis DJ (1985) Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 242:182-213.
29. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123-146.
30. LeDoux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8:2517-2529.
31. LeDoux JE, Farb C, Ruggiero DA (1990a) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043-1054.
32. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990b) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062-1069.
33. Linke R, Braune G, Schwegler H (2000) Differential projection of the posterior paralaminar thalamic nuclei to the amygdaloid complex in the rat. Exp Brain Res 134:520-532.
34. Liubashina O, Jolkkonen E, Pitkanen A (2000) Projections from the central nucleus of the amygdala to the gastric related area of the dorsal vagal complex: a Phaseolus vulgaris-leucoagglutinin study in rat. Neurosci Lett 291:85-88.
35. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
36. Maren S, Ferrario CR, Corcoran KA, Desmond TJ, Frey KA (2003) Protein synthesis in the amygdala, but not the auditory thalamus, is required for consolidation of Pavlovian fear conditioning in rats. Eur J Neurosci 18:3080-3088.
37. Martin JH (1991) Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett 127:160-164.
38. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332.
39. McDonald AJ, Augustine JR (1993) Localization of GABA-like immunoreactivity in the monkey amygdala. Neuroscience 52:281-294.
40. McGaugh JL, Ferry B, Vazdarjanova A, Roozendaal B (2000) Amygdala: role in modulation of memory storage. In: The amygdala: a functional analysis, Ed 2 (Aggleton JP, ed), pp 391-423. Oxford: Oxford UP.
41. Medina JF, Christopher Repa J, Mauk MD, LeDoux JE (2002) Parallels between cerebellum- and amygdala-dependent conditioning. Nat Rev Neurosci 3:122-131.
42. Muller J, Corodimas KP, Fridel Z, LeDoux JE (1997) Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111:683-691.
43. Nader K, Majidishad P, Amorapanth P, LeDoux JE (2001) Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 8:156-163.
44. Ono T, Nishijo H, Uwano T (1995) Amygdala role in conditioned associative learning. Prog Neurobiol 46:401-422.
45. Paré D, Smith Y (1993a) Distribution of GABA immunoreactivity in the amygdaloid complex of the cat. Neuroscience 57:1061-1076.
46. Paré D, Smith Y (1993b) The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience 57:1077-1090.
47. Paré D, Quirk GJ, LeDoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1-9.
48. Pascoe JP, Kapp BS (1985) Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 16:117-133.
49. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates: computer graphics files, compact Ed 3. San Diego: Academic.
50. Pitkanen A, Stefanacci L, Farb CR, Go GG, LeDoux JE, Amaral DG (1995) Intrinsic connections of the rat amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 356:288-310.
51. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4:724-731.
52. Royer S, Martina M, Paré D (1999) An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 19:10575-10583.
53. Royer S, Martina M, Paré D (2000) Polarized synaptic interactions between intercalated neurons of the amygdala. J Neurophysiol 83:3509-3518.
54. Samson RD, Paré D (2005) Activity-dependent synaptic plasticity in the central nucleus of the amygdala. J Neurosci 25:1847-1855.
55. Sanders SK, Shekhar A (1995) Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 52:701-706.
56. Schafe GE, LeDoux JE (2000) Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 20:RC96(1-5).
57. Schafe GE, Nader K, Blair HT, LeDoux JE (2001) Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 24:540-546.
58. Schwaber JS, Kapp BS, Higgins GA, Rapp PR (1982) Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 2:1424-1438.
59. Shi CJ, Davis M (1999) Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci 19:420-430.
60. Stevens CF (1994) CREB and memory consolidation. Neuron 13:769-770.
61. Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala's role in sensory processing. J Comp Neurol 313:295-325.
62. Uwano T, Nishijo H, Ono T, Tamura R (1995) Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala. Neuroscience 68:339-361.
63. Veening JG, Swanson LW, Sawchenko PE (1984) The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport- immunohistochemical study. Brain Res 303:337-357.
64. Walker DL, Davis M (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17:9375-9383.
65. Wilensky AE, Schafe GE, LeDoux JE (2000) The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J Neurosci 20:7059-7066.
66. Young BJ, Leaton RN (1996) Amygdala central nucleus lesions attenuate acoustic startle stimulus-evoked heart rate changes in rats. Behav Neurosci 110:228-237.